BIODIVERSITAS ISSN: 1412-033X Volume 19, Number 4, July 2018 E-ISSN: 2085-4722 Pages: 1303-1312 DOI: 10.13057/biodiv/d190417

The mangrove flora and their physical habitat characteristics in Bunaken National Park, North Sulawesi, Indonesia

RIGNOLDA DJAMALUDDIN Faculty of Fishery and Marine Science, Universitas Sam Ratulangi. Bahu, Malalayang, Manado 95115, North Sulawesi, Indonesia. Tel.: +62-431-868027, email: [email protected]; [email protected]

Manuscript received: 20 February 2018. Revision accepted: 14 June 2018.

Abstract. Djamaluddin R. 2018. The mangrove flora and their physical habitat characteristics in Bunaken National Park, North Sulawesi, Indonesia. Biodiversitas 19: 1303-1312. The mangrove forests of Bunaken National Park are among the most distinctive and unusual in Southeast Asia because of the species that the forests contain. This study investigated the identity and diversity of mangrove plants as well as physiographic factors and major physical processes of every type of sub-habitats. Seven surveys were conducted to collect and identify mangrove species of the park. Sub-habitats where specimen was found, aspects related to tidal inundation, nature of soil, freshwater influence and topography were observed as well as major physical processes influencing the condition of each sub- habitat. The results suggested that the park was floristically rich with at least 27 plant species and they were distributed over ten recognized sub-habitat types in different composition and diversity. Ceriops zippeliana Blume, Lumnitzera racemosa Willd, Lumnitzera littorea (Jack) Voigt., Sonneratia ovata Backer, and Camptostemon philippinense (Vidal) Becc. were found in Bunaken National Park and their presence confirmed the broader distribution limit of these species within Indo-Malesia region. A special notice was for C. philippinense as the distribution limit of this is rarely reported.

Keywords: Bunaken, Camptostemon philippinense, Ceriops zippeliana, Indo-Malesia, mangrove

INTRODUCTION Indonesia’s mangroves include two biogeographical regions, i.e., Indo-Malesia and Asia, Australasia and the Whatever the origin of the term of mangrove, whether it western Pacific (Duke et al. 1992). The lists of mangrove is derived from ‘mangle grove’ which refers to Rhizophora species within these regions have been improved by Duke mangle Linnaeus or from the old Malay words ‘mangin’ or et al. (1998) in which 50 mangrove species were found in ‘manggi-manggi’ (Claridge and Burnett 1993), or from the Indo-Malesia and 47 species in Australasia, including national language of Senegal ‘mangue’ (Vannucci 1998), several putative hybrids. However, 39 species were this term is now applied to those species, a relative small overlapped between the two biogeographical regions, thus group of higher plants, or the whole community of plants, the total number of species in both biogeographical regions which have been peculiarly successful in colonising is 57 species. Giesen et al. (2006) found that mangrove in tropical and sub-tropical intertidal habitats at the interface Indonesia has 48 species and in Bunaken National Park between land and sea (Clough 1979; Duke 1992; Maxwell alone, some 32 true mangrove species may be found 2015). Mangrove vegetation includes a range of functional (Tomlinson 1986), thus Indonesia has the highest forms, including trees, shrubs, palms and ground ferns mangrove diversity in Southeast Asia. (Duke et al. 1998). Mangrove can tolerate salt and brackish Oceanic circulations and climate regime may influence waters (Spalding et al. 1997), because the plants have the distribution of mangroves (Thom 1982). The marine developed complex morphological, anatomical, physiological, environment of Bunaken National Park is under the and molecular adaptations allowing survival and success in influence of dominant seawater mass coming from northern their high-stress habitat (Srikanth et al. 2015). Pacific Ocean to Indian Ocean flowing through Makasar Global distribution of mangrove has been explained in Strait that separates Sulawesi and Kalimantan (Van various reports (e.g. Giesen et al. 2006; Spalding et al. Bennekom 1988). The flow of seawater mass from 2010; Richards and Friess 2015; Hamilton and Casey northern Pacific is strengthened by the Mindanao Current 2016). Southeast Asia supports the world’s largest area of coming from the coastal areas in the southeast of the mangroves, originally extending over 5.1 million ha and Philippines Archipelago (Bingham and Lukas 1994). representing 33.5 % of the world’s total (Spalding et al. Climatically, the coastal environments of the park is 2010). The largest areas of mangrove in Southeast Asia are influenced greatly by the equatorial condition which is found in Indonesia (almost 60 percent of Southeast Asia's usually far from extreme climatic conditions with more total) (Giesen et al. 2006). In 2000 total mangrove area was proportion of wet season and little range of temperature estimated at approximate 2,788,683 ha with the percentage between 25.5C and 27.0C. of mangrove loss was of 1.72% between 2000 and 2012 The mangrove forests of the Bunaken National Park are (Richards and Friess 2015). among the most distinctive and unusual in Southeast Asia 1304 BIODIVERSITAS 19 (4): 1303-1312, July 2018 because of the species that the forests contain (Davie et al. the northern section (1034’48.8” N-124039’27.8” E; 1996; Djamaluddin 2004). It is believed that the interplay 1049’26.8” N-124051’32.4” E) and the southern section between geophysical, geomorphic and biological factors (1026’24.7” N-124039’24.7” E; 1016’50.5” N-124028’54.8” has supported the mangrove distribution and diversity in E). The total area covered by the northern sections was the intertidal environments of the park. This study 62,150 ha including the five islands of Bunaken, Siladen investigated mangrove species across various sub-habitat Manado Tua, Mantehage, Nain and the mainland coast types within the park, geographical distribution limits of between Tiwoho and Molas. The southern section was certain species within Indo-Malesia region, and spatial restricted to the mainland coast between the villages of distribution of mangrove species as the consequences of Poopoh and Popareng, covering a total area of 16,906 ha. species adaptation to major environmental conditions. Although the primary conservation concern responsible for the creation of the Park was the coral ecosystem, the reserve also supports about 2,000 ha of mangrove forests MATERIALS AND METHODS that includes 1,000 ha in Mantehage Island (Survey Area A1), about 200 ha between Molas and Tiwoho (Survey Study site and climate Area A2) and 800 ha between Poopoh and Popareng The Bunaken National Park is situated on the North (Survey Area B). A map of the study location and surveyed coast of Sulawesi Island. The Park consists of two sections, areas is provided in Figure 1.

Figure 1. The study areas of Bunaken National Park, North Sulawesi, Indonesia

DJAMALUDDIN – Mangrove of Bunaken National Park, North Sulawesi, Indonesia 1305

The rainfall in the study area is strongly affected by the Description and classification of mangrove sub-habitat wind systems. The north-westerly winds blow over the types South China Sea and bring moisture during September and A visual analysis of colored aerial photographs (1:6,000 April. In November these winds arrive in the North scale; taken in 1993) was conducted to describe general Sulawesi via the Sulawesi Sea and to the west coast of physical condition of mangrove ecosystems and to identify South Sulawesi in late of November or early of December. specific locations that were expected to have different Dry south-easterly winds blow from the wintery Australian physical conditions. Ground checks were made to ensure a land mass towards eastern Sulawesi. These dry winds cause representative sample was taken of all the various types of a short dry season in Manado from August to October. The environmental settings. Description and classification of total annual rainfall in northern section of the park reaches sub-habitat types were based primarily on dominant 3,000-3,500 mm with 2,200 mm during the wet season physical factors and processes including level of inundation (November-April) and 1,100 mm during the dry season in relation to elevation, local water circulation pattern, (May-October). In the southern section of the park, the freshwater inflow, and specific soil characteristics of rainfall is lower and ranges from 2,501-3,000 mm. The texture, salinity and field moisture content. The pattern of timing of the wet and dry season is the same as the north. seawater circulation was observed visually during ebb and Based on data of annual temperature during 1973-2016, the spring tides. The level of tidal inundation was determined annual temperature of North Sulawesi varied little between using a measuring stake. Soil samples were taken from ten 25.5 C and 27.0 C. The minimum annual mean sub-habitat types at three different times. Samples were temperature was 25.5 C recorded in 1984 and the taken at 0-300 mm depth at five random points in every maximum was 27.0 C occurred in 2015. type of habitat and these were pooled prior to laboratory analysis. Soil texture was determined using the pipette Specimen collection method. Soil salinity was measured using a Hand Seven surveys were carried out between November Refractometer (ARTAGO S/MILL) on the water samples 1995 and September 2016 to collect all mangrove of a known volume eluted through sediment samples. Soil specimens within the Bunaken National Park. The first Field Moisture Content (FMC) was determined using the survey was conducted between November and December procedure by Gardner (1965) based upon water lost from 1995 through a community-based survey (i.e., specimens the weight of soil samples oven-dried at 105 C to constant were collected by the local people) resulted in the weight. Biodiversity Professional (Version 2.0 ) was used collection of specimens of all plants recognized by the for Bray-Curtis Cluster Analysis with Sorensen similarity local people as separate species and for which they had to group sub-habitats based on species presence. All local names. The second survey was carried out in January sampling points for the observation of physical sub-habitat 1996 and the third survey in June 1999, in 23 locations in characteristics are shown in Figure 2. Survey Area A1, seven locations in Survey Area A2 and 36 locations in Survey Area B. Specimen collections in the second and third surveys were made after the sub-habitat RESULTS AND DISCUSSION descriptions were made. The fourth survey was conducted in January 2002 to confirm identification of a number of Mangrove flora species which were still uncertain in the previous surveys. There were 27 species from 12 families were found in The fifth survey was carried out between August 2002 and the mangrove forests of the Bunaken National Park (Table September 2004 in 10 locations of mangrove around 1). Tiwoho Village (Survey Area A2). The sixth survey was It was revealed from the Tiwoho survey (Survey Area conducted between October 2012 and October 2013 in the A2) that one specimen of C. zippeliana, formerly mangrove area between two islets in Mantehage Island recognized as C. decandra in the majority of its range (four locations in Survey Area A1). This sixth survey was (Sheue et al. 2009; Duke et al. 2010), was introduced in aimed to investigate the massive dieback of mangroves and early of 2000 but had never been successful in its natural possible new establishment of mangrove species. Four regeneration. B. cylindrica that were previously known to locations in mangrove areas between Poopoh and occur only at estuarine sub-habitat in Mantehage Island Pinasungkulan (Survey Area B) were also visited several (Survey Area A1) was found in the latest survey at times to check the presence of unrecorded species in the mangrove near Pinasungkulan (1022’56.4” N; previous surveys. The last survey was conducted in 124034’27.3”-Survey Area B) as young trees under canopy September 2016 to check the mangrove species species dominated by R. apiculata. One specimen of S. establishment at the restored site of Tiwoho (A2). Field ovata was also recorded, at a landward site with freshwater determination of the flora was based on morphological input, in Tiwoho (1035’31.0” N; 124050’37.9” E-Survey characteristics that were compared to a number of Area A2). references (e.g. Van Stennis 1955-58; Ding Hou 1958; There were five species not found in the mangrove Tomlinson 1986; Mabberley et al. 1995; Noor et al. 2006). forests of the Park compared with the broader longitudinal All the specimens used for determination of the flora were biogeographic region between 1200 and 1350 E defined by photographed and documented. All surveyed locations Tomlinson (1986). These species were Aegialitis annulata were presented in Figure 2. R. Browm, Aegiceras floridum Roemer & Schultes,

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Bruguiera exaristata Ding Hou, Bruguiera hainesii C.G. Park represents the northern distribution of this species Rodgers and Osbornia octodonta F. Muell. Later studies since it has not been reported here before (e.g., Chapman reported that species of A. floridum occurred in the 1970; Spalding et al. 1997). Compared to the distribution intertidal environment on Pulau Pondang (0025’00.3” N; limit of Lumnitzera sp. proposed by Excell (1954), the 124020’59.8” E) and O. octodonta in the intertidal habitat presence of L. littorea and L. racemosa in the study area within the area of Panua Nature Reserve (0027’45.3” N; confirmed that the broader distribution limit of these 121058'54.5" E). Both locations are situated in Tomini species within Indo-Malesia. Special notice was also drawn Gulf, to the east and south coast of the northern arc of to the presence of C. philippinense in this region since the Sulawesi Island (Damanik and Djamaluddin 2012; distribution limit of this species was rarely reported Djamaluddin 2015). In addition to the species in Table 1, (Chapman 1976; Tomlinson 1986). Individual trees of this there were several major associations of species including species occurred only at one small location in Mantehage Caesalpinia bonduc (Linnaeus) Roxb. (Fabaceae), Island (1042’59.4” N; 124045’31.2” E-Survey Area A1). Clerodendrum inerme (L.) Gaertn. (Verbenaceae), Hibiscus This location was expected to be the distribution limit of C. tiliaceus Linnaeus (Malvaceae), Scaevola plumieri philippinense since it was common only in the Philippines (Linnaeus) Vahl. (Goodeniaceae) and Terminalia catappa (Giaesen et al. 2006), although Mukhlisi and Sadiyasa Linnaeus (Combretaceae). (2014) reported tthe occurance his speciesin Berau of This study found new distribution of several other eastern Kalimantan (and in Donggala of western coast of species within the Indo-Malesia region since they have not Central Sulawesi (Wahyuningsih et al. 2012), but it was of been reported to occur in this region. These included C. absent from any reports of mangrove surveys in the south zippeliana (Ding Hou 1958); Lumnitzera sp. (Excell 1954); coast of northern Sulawesi (Damanik and Djamaluddin S. ovata (Chapman 1970); C. philippinense (Chapman 2012; Djamaluddin 2015) and the West Papua 1976). The occurrence of S. ovata in Bunaken National (Prawiroatmodjo and Kartawinata 2014).

Figure 2. Locations of plants collection and observation for physical sub-habitat characteristics in Bunaken National Park, North Sulawesi, Indonesia

DJAMALUDDIN – Mangrove of Bunaken National Park, North Sulawesi, Indonesia 1307

Table 1. The mangrove plants of Bunaken National Park, North Sulawesi, Indonesia

Family Species Local name Common name Acanthaceae Acanthus ilicifolius Linnaeus1 Gahana, Kammunte Holly mangrove Avicennia alba Blume2 Api-api Api-api putih Avicennia marina (Forssk.) Vierh1,2,3 Api-api Grey/white mangrove Bombacaceae Camptostemon philippinense (Vidal) Becc.1 Kayu pelompong - Combretaceae Lumnitzera littorea (Jack) Voigt.1,2 Lolang bajo Red-flowered black mangrove Lumnitzera racemosa Willd1 Lolang bajo putih White-flowered black mangrove Euphorbiaceae Excoecaria agallocha Linnaeus1,2,3 Buta-buta Milky mangrove, Blind-your-eye Meliaceae Xylocarpus granatum Kӧnig1,2,3 Kira-kira Cannonball mangrove Xylocarpus moluccensis Pierre2,3 Kira-kira Cedar mangrove Primulaceae Aegiceras corniculatum (Linnaeus) Blanco1,2,3 Rica-rica, Anting-anting River mangrove, Black mangrove Arecaceae Nypa fruticans (Thunb.) Wurmb.1,2,3 Bobo Mangrove palm Pteridaceae Acrostichum aureum Linnaeus1,2,3 Paku pece Golden mangrove fern Acrostichum speciosum Wildenow1,2,3 Paku pece Showy mangrove fern Rhizophoraceae Bruguiera cylindrica (Linnaeus) Blum1,3 Ting putih Large-leafed orange mangrove Bruguiera gymnorrhiza (Linnaeus) Lamk.1,2,3 Makurung laut Large-leafed orange mangrove Bruguiera parviflora Weight & Arnold ex Griffith3 Makurung Small-leafed orange mangrove Bruguiera sexangula (Lour.) Poir.3 Makurung darat Upriver orange mangrove Ceriops zippeliana Blume2 Ting papua Tengat merah Ceriopa tagal (Perr.) C.B. Robinson1,2,3 Ting biasa Rib-fruited yellow mangrove Rhizophora apiculata Blum1,2,3 Lolaro merah Corky stilt mangrove Rhizophora mucronata Lamk.1,2,3 Lolaro putih Upstream stilt mangrove Rhizophora stylosa Griffith1,2,3 Lolaro putih Long-styled stilt mangrove Rubiaceae Scyphiphora hydrophyllacea Gaertn.f.1,2,3 Lemong pece Yamstick mangrove Lythraceae Sonneratia alba J. Smith1,2,3 Posi-posi White-flowered apple mangrove Sonneratia caseolaris (Linnaeus) Engler2 Posi-posi Red-flowered apple mangrove Sonneratia ovata Backer2,3 Posi-posi Ovate-leafed apple mangrove Sterculiaceae Heritiera littoralis Dryand1,2,3 Kolot kambing Looking-glass mangrove Note: 1) species found in mangroves of Mantehage Island, Survey Area A1, 2) species found in mangrove of coastal mainland between Molas and Tiwoho, Survey Area A2, 3) species found in mangrove between Poopoh and Popareng in the southern section of the Park, Survey Area B

Sub-habitat types and their physical characteristics inland fringe (sub-habitat 9) and a seasonal or regular Mangroves within the Park were found to occupy at freshwater influenced landward fringe (sub-habitat 10). least ten different types of sub-habitat based primarily on Characteristics of each sub-habitat type in relation to physical conditions and processes. Generally, these ten various conditions of physical environment are presented in sub-habitats could be classified into two main groups, i.e., Table 2. estuarine and coastal mangrove ecosystems. Based on the Sub-habitat 1 was located in the center of Mantehage elevation relative to the sea level, estuarine mangrove Island (Figure 2). This was subjected to sedimentation from comprised of up and intermediate locations. Whereas nearby land systems and under influence of seasonal coastal mangrove ecosystems comprised of three freshwater inflow from run-off. There were two deepest recognizable elevations, i.e., low, intermediate and high parts or undeveloped lagoons located near the center of this elevations. How these ten sub-habitat types were sub-habitat. As this was only reached by seawater at high categorized, as well as their relative position across the tide, surface substrate of areas around the lagoons might be mangrove forest of Bunaken National Park is presented in drier due to excessive evaporation. In contrast, these areas Figure 3. could be inundated by freshwater during wet season. As can be seen from Figure 3 that there was an estuary Sub-habitat 2 was common type in the Mantehage (sub-habitat 1) in the Park. At low elevation four types of Island and coastal mainland. This was located at about sub-habitat were recognized; seaward fringe (sub-habitat Mean Seawater Level (MSL), being inundated up to 77 2), coralline sand berm (sub-habitat 3), tidal water times month-1. Its extent depended upon the topography of impoundment (sub-habitat 4) and seaward young soil (sub- a mangrove forest. The flatter a mangrove forest the wider habitat 5). At intermediate elevation, there were two major the habitat will be. In the Mantehage Island, most of the sub-habitat types of very stable and flat middle zone (sub- mangrove forest was narrow with the exception for the habitat 6) and tidal stream edge (sub-habitat 7). But sub- mangrove area in the north side which was subjected to habitat 7 was also found at high elevation. Three other sedimentation and had a relatively flat topography. Another main sub-habitat types comprised of less steep slope and typical characteristic of this sub-habitat was of the absence eroding landward fringe (sub-habitat 8), a highly accreting of freshwater inflow.

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Figure 3. Estuarine and coastal locations of mangrove sub-habitats in Bunaken National Park, North Sulawesi, Indonesia (the terms up and intermediate for sub-habitat; and low, intermediate and high for sub-habitat 2-10 refers to the elevation of these habitats relative to sea level)

Sub-habitat 3 was found in the mangrove islands to the Sub-habitat 6 was the most common habitat, comprised north of Mantehage Island and the mangrove island of up to 50% of the total mangrove forests. This sub-habitat Tatapaan in the southern section of the Park. This sub- type was located at intermediate elevation relative to sea habitat type was characterized by its coral sand berm level and was inundated up to 53 times month-1 but sediments lying on dead coral reef, convex form of freshwater influence was of insignificant. The sediment topography and low elevation relative to sea level. Most was dominated by organic matter. areas of this sub-habitat were inundated at almost all time Sub-habitat 7 was common in the southern part of the and no freshwater supply into this sub-habitat. park where tidal channel components usually dissect the Sub-habitat 4 was found at one location, near Tanjung mangrove belt. This sub-habitat type could be found from Pasir Putih, in the southern part of the park. Due to its intermediate to high elevation along a tidal channel in concave topography, this sub-habitat was permanently which bank was prograded at one side and eroded at inundated including during low tide level. The sediment another. Level of tidal inundation varied along the tidal mainly composed of fine and well-draining sand and small channel depended on the position of the sub-habitat at proportion of organic matter and the water was mixed with intermediate or high elevation. Seasonal freshwater the freshwater from seepage and run-off. influence from seepage and run-off was significant at high Sub-habitat 5 was another type of mangrove islands. elevation near the coastline. This was located just in the front of the seaward end of Sub-habitat 8 was of common habitat over the tidal channel of the mangrove forest near Sondaken Village mangrove forest in the park. This habitat located at high in the southern part of the park. Overwash, formed by the elevation relative to sea level and was inundated up to 10 accumulation of mostly non-organic sediment transported times month-1. Topography of this habitat was usually in through the tidal channel was in the low elevation. No less steep slope. Freshwater might influence this habitat freshwater was observed to influence this sub-habitat. from seepage and run-off at seasonal period.

DJAMALUDDIN – Mangrove of Bunaken National Park, North Sulawesi, Indonesia 1309

Sub-habitat 9 occurred at the inland mangrove area substrate was always wet and deep. This habitat was between Rap-rap and Sondaken in the southern part of the inundated up to 10 times month-1 and received supply of park that was subjected to massive sedimentation from the freshwater at regular basis. near land. This habitat was at high elevation relative to sea Textural classes of surface substrate seemed clearly level, the surface of substrate was not smooth as it had different between certain sub-habitats whilst others many mounds and was inundated only at maximum high appeared to be relatively the same (Figure 4). For example, spring tide. Freshwater might flowed seasonally from the sub-habitat 1 and 6 had a texture dominated by silt particle nearest land through seepage and run-off. (silt loam texture). On the other hand, sub-habitat 2, 7 and Sub-habitat 10 located at high elevation relative to sea 10 had loam texture. Sub-habitat 9 was composed of sandy level and had a flat to less steep topography. Surface loam clay.

Table 2. Physical characteristics of sub-habitat types in Bunaken National Park, North Sulawesi, Indonesia

Elevation Local Level of Freshwater Habitat types relative to sea Sediment feature topography inundation influence level Estuary Up and Basin with Frequently Fine and deep clay and poorly Seasonal (Sub-habitat 1) intermediate isolated lagoon waterlogged, drained surface substrate, inundated at salinity (21.7±7.4 ppt), textural spring tide type (silt), FMC (534.0±4.5%) Seaward fringe Low Flat to less steep Inundated at Sand with small portion of fine Absent (Sub-habitat 2) almost all tide sediment, salinity (14.0±0.0 levels (77 times ppt), textural type (loam), FMC month-1) (174.0±3.3%) Coralline sand Low Convex Inundated at Coralline sand berm, Absent berm (Sub-habitat almost all tide salinity (8.0±0.0 ppt), textural 3) levels (77 times type (sandy loam), FMC month-1) (39.0±4.3%) Tidal-water Low Concave Inundated at low Fine and well-draining sand From seepage impoundment tide (up to 107 with little proportion of organic and run-off (Sub-habitat 4) times month-1) matter, salinity (13.3±0.5 ppt), textural type (sandy loam), FMC (78.3±1.2%) Seaward young Low Convex Inundated at all Subjected to accumulation of Absent soil (Sub-habitat 5) the time (77 mostly non-organic fine times month-1) sediments, salinity (18.0±0.0 ppt), textural type (sandy loam), FMC (219.3±3.3%) Very stable middle Intermediate Less steep Inundated at Dominated by organic sediment, Not zone (Sub-habitat normal high tide salinity (19.7±1.2 ppt), textural significant, 6) (53 times month- type (silt loam), FMC from seepage 1) (244.0±3.7%) and run-off Tidal-stream edge Intermediate and Various Various Salinity (18.0±0.8 ppt), textural Seasonally or (Sub-habitat 7) high (Prograding and depending on type (loam), FMC (201.0±2.2 regularly from eroding banks) local positions %) seepage and (intermediate, run-off high) especially at high position Less steep and High Less steep Inundated by Shallow surface substrate and in Seasonal from eroding landward tidal water up to many cases excessively eroded, seepage and fringe (Sub-habitat 10 times month-1 salinity (19.0±0.0 ppt), textural run-off 8) type (sandy loam), FMC (207.3±2.1 %) Highly accreting High Not smooth Inundated at Dry and subjected to Seasonal from inland fringe (Sub- surface with maximum high sedimentation from nearest seepage and habitat 9) many mounds tide (4 times land, salinity (14.3±0.5 ppt), run-off month-1) textural type (sandy loam), FMC (90.7± 2.9 %) Seasonally or High Flat to less steep Inundated 10 Wet and deep, salinity (6.5±0.5 Regular regularly times month-1 ppt), textural type (loam), FMC freshwater (83.3±2.5 %) influenced landward fringe (Sub-habitat 10)

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Figure 4. Surface soil texture composition of the sub-habitats in Figure 6. Surface soil field moisture content of the ten sub-habitat Bunaken National Park, North Sulawesi, Indonesia types

Based on surface soil salinity the ten sub-habitats could Species diversity over various sub-habitat types be divided into three groups (Figure 5). The first group of All ten recognized sub-habitat types had different sub-habitats was with high soil salinity varied between 18.0 species diversity (Table 3). Based on the number of species and 21.7 ppt, including sub-habitat 5, 6, 7and 8. The present, sub-habitats could be divided into four categories. second group of sub-habitats was with intermediate soil The first category included the high diversity sub-habitat salinity ranging from 13.3 ppt to 14.0 ppt, including sub- which was found on sub-habitat 10 with 14 species. The habitat 1, 2, 4 and 9. The third group of sub-habitats was second category was a group of sub-habitats that contained with relatively low soil salinity varied between 6.5 and 8 9 species including sub-habitat 1, 9, 7 and 10. This ppt, including sub-habitat 3 and 10. As indicated by the category was defined as a moderate species diversity sub- value of standard deviation, surface soil salinity of sub- habitat. The third category was the sub-habitat 2, 3, 4 and 5 habitat 1 seemed to be more varied. In mangroves, extreme that contained 4-6 species and defined as low species substrate salinity induces hydraulic failure and ion excess diversity. The sub-habitat 6 was the only sub-habitat with toxicity and reduces growth and survival (Méndez et al. two species present and defined as poor species diversity. 2016). Field moisture content measured in the ten sub-habitats Table 3. Mangrove species within varieties of sub-habitat types in varied greatly (Figure 6). The highest value was measured Bunaken National Park, North Sulawesi, Indonesia for sub-habitat 1 at 534.0 %. The sub-habitat 2, 5, 6, 7 and Sub-habitat Types 8 had field moisture varying between 174.0 and 244.0 %. Species Sub-habitats that had field moisture less than 100 % were 1 2 3 4 5 6 7 8 9 10 measured for sub-habitat 3 (39.0 %), sub-habitat 4 (78.3 A. ilicifolius + + + A. aureum + + + + %), sub-habitat 9 (90.7 %) and sub-habitat 10 (83.3 %). A. speciosum + + + + These differences were probably to be associated with A. corniculatum + + differences in sand composition in which field moisture A. alba + content tended to decrease with the increased in the number A. marina + + + + + + + + of sand particles (Djamaluddin 2004). B. cylindrica + B. gymnorrhiza + + + + + B. parviflora + +

B. sexangula +

C. philippinense + C. zippeliana + C. tagal + + + + E. agallocha + + H. littoralis + + L. littorea + L. racemosa + N. fruticans + + R. apiculata + + + + + + + + R. mucronata + + + + R. stylosa + + + + S. hydrophyllacea + S. alba + + + + S. caseolaris + S. ovata + X. granatum + + Figure 5. Surface soil salinity of the ten habitat types in Bunaken X. molluccensis + + + Total 9 6 6 5 4 2 9 14 9 9 National Park, North Sulawesi, Indonesia

DJAMALUDDIN – Mangrove of Bunaken National Park, North Sulawesi, Indonesia 1311

Figure 7. Groups of sub-habitats based on composition of species presence

Based on composition of species present, the ten sub- waterlogged and inundated by seawater only at high spring habitats could also be classified into four groups (Figure 7). tide. Those physical features were predicted to be the most The first group consisted of sub-habitat 1, 9 and 10. This likely factors that supported the growing of two dominant group was characterized by the presence of species of A. canopy species of B. cylindrica and L. racemosa. Several ilicifolius, A. aureum, A. speciosum, A. marina and N. species such as A. marina, E. agallocha, and R. apiculata fruticans. The second group consisted of sub-habitat 7 and were also found on some particular points along the tidal 8 that was characterized by the presence of A. streams of this sub-habitat. According to Duke et al. corniculatum, A. marina, B. gymnorrhiza, C. tagal, R. (1998), the physiological tolerance of each mangrove apiculata, X. granatum, X. moluccensis. The third group species to salinity influences its estuarine distribution. consisted of sub-habitat 2, 3, 4 and 5. The presence of three Unlike the estuarine sub-habitat, the physical attributes species of Rhizophora (R. apiculata, R. mucronata, and R. of the tidal-stream edge sub-habitat were largely controlled stylosa) and S. alba were of typical in these sub-habitats. In by seawater flowing through the tidal stream. Surface soil this group, sub-habitat 2 and 3 were exactly the same in texture was mostly composed of sandy clay loam. This term of the presence of A. marina and B. gymnorrhiza. The habitat was quite saline as shown by the surface salinity fourth group consisted of sub-habitat 6 that was characterized ranged from 17 to 19 ppt. These particular environmental by the presence of R. apiculata and B. gymnorrhiza. characteristics were probably the factors that supported the Across the intertidal zone of the park, the composition survival of A. marina, B. parviflora, C. tagal, Xylocarpus of mangrove species appeared to vary with types of sub- granatum and X. Mollucensis especially the two dominant habitat. The seaward mangrove areas comprised of sub- species of R. apiculata and B. gymnorrhiza. habitat 2, 3, 4 and 5. These sub-habitats occupied by Overall, A. marina and R. apiculata had very broad Rhizophora spp. (R. apiculata, R. mucronata, R. stylosa) spatial distribution, while a number of species such as A. and S. alba. However, B. gymnorrhiza was also found on ilicifolius, A. corniculatum, A. alba, B. cylindrica, B. sub-habitat 2 and 3. The low ground slope appeared to be a parviflora, B. sexangula, C. philippensis, H. littoralis, L. likely reason for the similarity of these sub-habitats. The littorea, N. fruticans, S. hydrophyllacea, S. caseolaris, S. middle mangrove areas included sub-habitat 6 and 7 ovata, X. Granatum had very limited spatial distribution in (particularly its intermediate position). R. apiculata and B. which each of these species occupied only one or two gymnorrhiza dominated on sub-habitat 6. The presence of a habitat types. In addition, Acrostichum aureum and A. high proportion of clay particles in the surface soil seemed speciosum, three species of Rhizophora (R. apiculata, R. to be characteristic of this sub-habitat. The landward mucronata, R. stylosa), and two species of Xylocarpus (X. mangrove areas had a variety of sub-habitats including sub- granatum and X. moluccensis), often occurred sympatrically. habitat 8, 9 and 10. C. tagal appeared to be dominant in However, the four species of Bruguiera (B, cylindrica, B. sub-habitat 8 and 10, but not in sub-habitat 9. Beside C. gymnorrhiza, B. parviflora, B. sexangula), two species of tagal, a number of species such as A. marina, B. sexangula, Lumnitzera (L. littorea and L. racemosa), three species of N. fruticans and S. ovata usually occurred on sub-habitat Sonneratia (S. alba, S. caseolaris, S. ovata), occupied 10. The variation in surface soil salinity might be a clearly different types of sub-habitat. With particular defining feature of the landward mangrove areas. concern to three species of Rhizophora, the most widely The estuarine sub-habitat located in the center between distributed mangrove trees in the Indo-West Pacific region the two islets on Mantehage Island was considered to be (Yan et al. 2016), natural hybridization was more likely to different from other sub-habitat types. Physically this sub- occur where parental species of Rhizophora could occur habitat was poorly drained, subjected to being frequently (e.g. Setyawan et al. 2014; LungNg and Szmidt 2015).

1312 BIODIVERSITAS 19 (4): 1303-1312, July 2018

Finally, the mangrove flora in Bunaken National Park Duke N, Kathiresan K, Salmo III SG, Fernando ES, Peras JR, Sukardjo S, was floristically rich with at least 27 species, and the Miyagi T. 2010. Ceriops zippeliana. IUCN Red List of Threatened Species Version 2014.3. International Union for Conservation of broader northern distribution limit of L. littorea and L. Nature and Natural Resources. racemosa, C. philippinense, S. ovata was confirmed. The Duke NC, Ball MC, Ellison JC. 1998. Factors influencing biodiversity and presence of C. philippinense was of importance since distributional gradients in mangroves. Glob Ecol Biogeogr Lett 7: 27-47 report of this species was rare. Mangrove species were Duke NC. 1992. Mangrove floristics and biogeography. In: Robertson AI, Alongi DM (eds). Coastal and Estuarine Studies. American distributed over at least ten sub-habitat types in different Geophysical Union, Washington. identity and diversity. The low ground slope appeared to be Excell AW. 1954. Combretaceae. Flora Malesiana 1 (4): 533-89. a likely reason for the similarity of four sub-habitat types in Fernado S, Pancho JV. 1980. Mangrove trees of the Philippines. Silvatrop the seaward mangrove area. The presence of a high Philippine For Res J 5: 35-54. Gardner, W. H. (1965). Water content. In: Black CA (ed). Methods of Soil proportion of clay particles in the surface soil seemed to be Analysis: Part I Physical and Mineralogical Properties. American characteristic of two sub-habitat types (a flat middle zone Society of Agronomy, Wisconsin. and a tidal stream edge) in the middle mangrove area. The Giesen W, Wulffraat S, Zieren M, Scholten L. 2006. Mangrove variation in surface soil salinity might be a defining feature Guidebook for Southeast Asia. Food and Agriculture Organization of the United Nations Regional Office for Asia and the Pacific, of three sub-habitat types in the landward mangrove area. Bangkok. Poor drainage, being frequently waterlogged and inundated Hamilton SE, Casey D. 2016. Creation of a high spatiotemporal resolution by seawater only at high spring tide seemed to be a global database of continuous mangrove forest cover for the 21st characteristic of estuarine sub-habitat. Meanwhile, a sandy century (CGMFC-21). Glob Ecol Biogeogr 25 (6):729-738. LungNg W, Szmidt A. 2015. Introgressive hybridization in two Indo-West clay loam of soil texture and a relatively high surface soil Pacific Rhizophora mangrove species, R. mucronata and R. stylosa. salinity were the physical attributes of a tidal-stream edge Aquat Bot 120: 222-228. sub-habitat. Mabberley CM, Pannel CM, Sing AM. 1995. Flora Malesiana: Seri I Spermathophyta 12 (1): 371-81. Maxwell GS. 2015. Gaps in mangrove science. ISME/GLOMIS 13 (5): 18-38. ACKNOWLEDGEMENTS Méndez AR, López PJ, Moctezuma C, Bartlett MK, Sack L. 2016. Osmotic and hydraulic adjustment of mangrove saplings to extreme salinity. Tree Physiol. 36 (12): 1562-1572. Financial support had come from USAID-NRM to Mukhlisi, Sidiyasa K. 2014. Structure and composition of mangrove conduct mangrove ecological study from November to species in Berau Mangrove Information Centre (PIM), Kalimantan December 1995, subsequently from Australian Agency for Timur. Indonesian For Rehabil J 2 (1): 25-37. [Indonesian] International Development (AusAid), Mangrove Action Noor YR, Khazali M, Suryadiputra INN. 2006. Mangrove introduction guide. Ditjen PPHKA-Wetland International, Bogor. [Indonesian] Project (MAP), Rufford Small Grant (RSG), Whitley Fund Percival M, Womersley JS. 1975. Floristics and ecology of the mangrove for Nature (WFN), Global Environmental Fund-Small vegetation in Papua. New Guinea Bot Bull 8. Grants Programme (GEF-SGP), Balai Taman Nasional Prawiroatmodjo S, Kartawinata K. 2014. Floristic diversity and structural Bunaken. I am sincerely indebted to Dr. Jim Davie, Ass. characteristics of mangrove forest of Raja Ampat West Papua, Indonesia. Reinwardtia 14 (1):171-180. Prof. David Lamb, Prof. Eugene Moll, Dr. Norman Duke Richards DR, Fries DA. 2016 Rates and drivers of mangrove deforestation for their constructive criticisms during the course of my in Southeast Asia 2000-2012. Proc Natl Acad Sci USA 113 (2): 344-349. work, to Mr. Brama Jabar in providing the map of study Setyawan AD, Ulumuddin YI, Ragavan P. 2014. Review: Mangrove location and to Christopher Minor for English check. hybrid of Rhizophora and its parental species in Indo-Malayan region. Nusantara Biosci 6 (1): 69-81. Sheue CR, Liu HY, Tsai CC, Rashid SMA, Yong JWH, Yang YP. 2009. On the morphology and molecular basis of segregation of Ceriops REFERENCES zippeliana and C. decandra (Rhizophoraceae) from Asia. Blumea 54: 220-227. Spalding MD, Blasco F, Field CD. 1997 World Mangrove Atlas. Bingham FM, Lukas R. 1994. 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